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Annals of Botany 77: 547-553, 1996
BOTANICAL BRIEFING
Pattern in the Root Epidermis: An Interplay of Diffusible Signals
and Cellular Geometry
LIAM DOLAN
Department of Cell Biology, John Innes Centre, Norwich NR4 7UH, UK
Received: 22 November 1995 Accepted: 14 January 1996
The epidermis of roots is composed of hair and non-hair cells. Patterning of this epidermis results from spatially
regulated differentiation of these cell types. Root epidermal development in vascular plants may be divided into three
broad groups based on the mode of hair development; Type 1: any cell in the epidermis can form a root hair; Type
2: the smaller product of an asymmetric cell division forms a root hair; Type 3: the epidermis is organized into discrete
files of hair and non-hair cells. The Arabidopsis root epidermis is composed of discrete files of hair and non-hair cells
(Type 3). Genetic and physiological evidence indicates that ethylene is a positive regulator of hair cell development.
Genes with opposite roles in the development of hair cells in the shoot (trichomes) and hair cells in the root have been
identified. Plants with presumptive loss of function alleles in the TRANSPARENT
TESTA GLABRA (TTG) or
GLABRA2 (GL2) genes are devoid of trichomes indicating that these genes are positive regulators of trichome
development. The development of supernumerary root hair cells in these mutant backgrounds illustrates that these
genes are also negative regulators of root hair cell development. A model that explains the spatial pattern of epidermal
cell differentiation implicates ethylene or its precursor 1-amino-l-cyclopropane carboxylate as a diffusible signal.
Possible roles for the TTG and GL2 genes in relation to the ethylene signal are discussed.
© 1996 Annals of Botany Company
Key words: Arabidopsis, root development, ethylene, root hair cell, epidermis.
INTRODUCTION
Cell patterning in the root epidermis
The root epidermis of most vascular plants is composed of
a patterned array of two cell types, root hair cells and nonhair cells. The development of hair cells has been described
on roots and root-like structures of the most primitive,
extant, vascular plants, such as Lycopodium, Selaginella and
through to the most advanced groups of angiosperms
(Leavitt, 1904). Recently, the genetic analysis of root
epidermal pattern in Arabidopsis has led to a mechanistic
understanding of the patterning process in this species and
sets the stage for its examination in other taxa with different
epidermal patterns.
In a survey of the organization of cells in the root
epidermis of extant members of most groups of vascular
plants, Leavitt (1904) distinguished between two basic
patterns of epidermal differentiation; Type 1 (Fig. 1A): any
cell in the root epidermis may differentiate as a root hair
cell, Type 2 (Fig. IB): root hair cells differentiate from the
smaller product of an asymmetric cell division in the
meristematic zone (Cormack, 1937; Cutter and Feldmann,
1970; Cutter and Hung, 1972). Cormack (1935, 1947)
described what might be considered to be a third pattern,
Type 3 (Fig. 1C): epidermal cells arranged in files composed
of only one cell type, either hair cells or non-hair cells.
Species in which hair cells differentiate in any position (Type
1) are characteristic of most ferns (Filopsida), some
monocotyledons and almost all dicotyledons. The second
0305-7364/96/060547 + 07 $18.00/0
type of differentiation is characteristic of more primitive
land plants such as Lycopodium, Selaginella, Isoetes
(Lycopisda), Equisetum (Sphenopsida) and some monocotyledons and a single dicotyledonous family, the
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FIG. 1. Three types of root epidermal patterning in mature roots of
vascular plants. Black cells are non-hair cells and hatched cells are root
hair cells. The circle represents the position of the root hair base. A,
Type 1 differentiation in which any hair can form a root hair. B, Type
2 differentiation in which root hair cells are the smaller product of an
asymmetric cell division in the meristem. C, Type 3 differentiation in
which there are discrete files of hair cells and files of non-hair cell files.
© 1996 Annals of Botany Company
548
Dolan—Pattern in the Root Epidermis
Nymphaeaceae. Type 3 differentiation is found among
members of the Brassicaceae.
PATTERN
Cell patterning as a developmental process
Pattern is defined as the three-dimensional spatial arrangement of pattern elements. In the root epidermis, a twodimensional system, the elements are individual cells. In
other systems the pattern elements may include branches (in
establishing the architectural model of the shoot system),
leaves (phyllotaxis), floral organs (in a flower), etc. Celltypes in the root epidermis may be located in any position
relative to neighbouring cells (Type 1), regularly spaced
along all cell files as a result of regular asymmetric cell
divisions (Type 2) or in an array where cells are arranged in
files of identical cell types (Type 3) (Leavitt, 1904; Cormack,
1935, 1947).
While studying the development of pattern at the level of
individual cells may at first glance appear to have little to do
with the patterning of other ' big' plant structures such as
leaves and flowers, it should be remembered that many of
the interactions that occur during the development of these
' big' structures take place over relatively few cell distances
at or near the meristem or in developing primordia.
Therefore the mechanisms that govern the patterned
specification of cell fate in an epidermis may, theoretically at
least, be similar to those that are involved in the patterning
of larger structures. In a similar vein, both anterior-posterior
and dorso-ventral polarity in the Drosophila embryo is
established over one cell distance, between the oocyte and
the surrounding follicle cells (Gonzalez-Reyes, Elliot and St
Johnson, 1995).
Cell fate in plants has been shown in numerous studies to
be dependent on position and not lineage (Barlow, 1984;
Steeves and Sussex, 1989; Irish, 1991; van den Berg et al.,
1995). Another way of saying this is that cell fate is
determined relatively late in development and is dependent
upon cues received by a cell from its environment and
neighbours. This is not to say that dividing cells are not
TABLE
responding to cues, rather it indicates that these cues may be
overridden by other signals to which the cells are exposed
later in development. The aim of the present research is to
identify these developmental signals and characterize their
role in the patterning of the root epidermis.
Genetic analysis facilitates the identification of molecules
that are involved in the development of cell pattern
Genetic analysis allows the identification of genes that
encode proteins that are involved in a developmental
process. A change in the DNA sequence of a gene or its
regulatory region is known as a mutation. Genes involved in
specific aspects of development may be identified by
mutation. For example, if the activity of a particular gene
required for hair development (a positive regulatory gene) is
lost, by mutation, then the plant carrying the mutation will
exhibit a hairless phenotype. Therefore screening populations of mutant seedlings for root-hairless phenotypes
would identify genes which are positive regulators of hair
development. If on the other hand one were to screen for
extra-hairy mutant seedlings then one might expect to
identify mutations in negative regulatory genes. Such loss of
function mutations are generally recessive to the wild-type
gene, i.e. heterozygous plants (carrying one wild-type and
one mutant copy of the gene) are wild-type in phenotype. A
list of the mutant genes and their proposed roles in root
epidermal patterning is presented in Table 1.
CELL P A T T E R N I N G IN THE
ARABIDOPSIS
ROOT E P I D E R M I S
The primary root of Arabidopsis is structurally simple and
invariant (Dolan et al, 1993). It consists of a stele encircled
by an eight-celled endodermis and cortex. The cortex is in
turn encircled by an epidermis which is composed of two cell
types. Epidermal cells lying over the anticlinal (wall
perpendicular to the root surface) cortical cell walls form
root hairs (Dolan et al., 1994; Galway et al., 1994).
Epidermal cells located over the outer periclinal wall (wall
1. List of genes involved in patterning the root epidermis in Arabidopsis
Gene
Mutant phenotype
CONSTITUTIVE
TRIPLE RESPONSE]
(CTRI)
Root hairs develop in all
cell files in root epidermis
TRANSPARENT
TESTA GLABRA
(TTG)
GLABRA2 (GL2)
Root hairs develop in all
root hair files in epidermis
ROOT HAIR
DEVELOPMENT6
(RHD6)
DWARF (DWE)
AUXIN RESISTANT2
(AXR2)
Proposed wild-type
function
Reference
Negative regulator of root
hair development and
ethylene signal
transduction
Negative regulator of root
hair development
Kieber et al., 1993;
Dolan et al., 1994
Root hairs develop in all
hair files of epidermis
Few root hairs develop
Negative regulator of root
hair development
Positive regulator of root
hair development
Dolan and Morelli
(unpubl. res.)
Masucci et al., 1994
No root hairs develop
Positive regulator of root
hair development
Mirza et al., 1984
No root hairs develop
Galway et al, 1994
Wilson et al., 1990
549
Dolan—Pattern in the Root Epidermis
parallel to the root surface) of a single cortical cell form
non-hair cells. Cell fate in the root epidermis is therefore
defined by the relative position of epidermal cells and their
neighbours.
Histological and clonal analysis has indicated that the
root epidermis is derived from a ring of approximately 16
initials located below the quiescent centre at the root tip
(Dolan et al, 1993, 1994). Clonal analysis allows the fates of
cells to be determined since it involves the uncovering of a
genetic marker in cells that is inherited in all descendent
cells. The uncovering of a histochemical GUS (glucuronidase) marker (introduced on a transgene) in epidermal
initial cells results in a clone of cells in the lateral root cap
and adjacent epidermis being labelled with GUS activity.
This provides unequivocal evidence that the epidermis and
lateral root cap are derived from a common set of initials in
Arabidopsis (Dolan et al., 1994).
Differences between the two epidermal cell types are
evident early in their development in the Arabidopsis root
epidermis (Dolan et al., 1994; Galway et al., 1994). Hair
cells are shorter than their neighbouring non-hair cells by
the time they undergo elongation so that the root hair cell
is generally shorter than the non-hair cell at maturity.
Cytoplasmic vacuolation of the non-hair cells is evident
before it occurs in the hair cells giving them the relatively
dense cytoplasmic appearance (Dolan et al., 1994; Galway
et al., 1994). Bulges appear at the end of the root hair cell
nearest the meristem by the end of the elongation stage
(Dolan et al, 1994; Masucci et al., 1994). The growth of the
bulge is initially slow (< 1 /an h"1) but gradually increases
to about 1 fim min"1 once the hair attains a length of
approximately 20 [im. (Dolan et al., 1994). Consequently,
the hair cell is actively growing at this stage of development,
while the non-hair cells of the epidermis have ceased
growth. The uncoupling of growth in these cell types is
accompanied by the loss of symplastic continuity between
the two cell types (Duckett et al, 1994). It is therefore
possible that cell signalling events involving plasmodesmatal
movement of symplastic signals may play a role in the
specification of cell fate in this tissue.
Ethylene is a positive regulator of root hair development in
Arabidopsis
Ethylene is involved in a large number of developmental
and stress related processes in plants (reviewed in Abeles,
1973; Yang and Hoffman, 1984; Kieber and Ecker, 1993;
Zarembinski and Theologis, 1994; Ecker, 1995). Its biosynthetic pathway has been characterized in great detail and
permits experimental manipulation of ethylene biosynthesis
and perception (Yang and Hoffman, 1984). Methionine
adenosyl transferase converts methionine to S-adenosyl
methionine which is converted to 1-aminocyclopropane-lcarboxylate (ACC) by ACC synthase which is inhibited by
aminoethoxyvinylglycine (AVG) (Adams and Yang, 1979;
Liang et al, 1992; Rodrigues-Pousada et al, 1993). ACC is
in turn converted to ethylene by ACC oxidase (Hamilton,
Bouzayen and Grierson, 1991). The perception of ethylene
is blocked by Ag+ which is thought to inhibit the binding of
ethylene to its receptor (Beyer, 1976). The ethylene signal
ACC
ACC
FIG. 2. Changes in the pattern of epidermal cell differentiation in
different roots. A, Wild-type root in which root hair cells (hatched) are
located in the cleft over the anticlinal walls of underlying cortical cells
(white) and non-hair cells (black) are located over the outer periclinal
walls of cortical cells. B, The phenotype of Ctrl roots in which hair cells
(hatched) differentiate in the position normally occupied by non-hair
cells. C, Epidermal pattern in roots treated with the positive regulator
of root hair development, ACC, showing hair cells (hatched) in the
locations normally occupied by non-hair cells. D, The epidermis of
roots treated with the inhibitor of ethylene biosynthesis AVG is
composed entirely of non-hair cells.
transduction pathway has been characterized genetically
and provides a number of mutant backgrounds in which to
examine the role of ethylene in epidermal development
(Bleecker et al, 1988; Guzman and Ecker, 1990; Harpham
et al, 1991; van der Straeten et al, 1993; Roman et al,
1995).
Plants
carrying
recessive
mutations
of
the
CONSTITUTIVE
TRIPLE
RESPONSE1 gene of
Arabidopsis have short hairy roots indicating that the wildtype gene is a negative regulator of root hair cell development
(Fig. 2B) (Kieber et al, 1993). Ctrl plants behave as though
they constitutively respond to ethylene in so far as they have
an exaggerated hypocotyl hook, short hypocotyl and root
when grown in the darkness. Sectioning of these Ctrl roots
reveals that these roots appear hairy not only because the
epidermal cells are short resulting in the development of a
larger number of root hairs per unit length of root, but also
because a large portion of the hair cells develop in ectopic
locations (over the periclinal walls of underlying cortical
cells) (Dolan et al, 1994). Since the CTR1 gene is a negative
regulator of the ethylene response it follows that ethylene is
probably a positive regulator of root hair cell development.
The CTR1 gene encodes a kinase of the Raf family
(Kieber et al, 1993). Such proteins may be involved in
signalling through a number of distinct signalling cascades
within an individual cell (Neiman, 1993). It was therefore
necessary to show that ethylene is a positive regulator of
hair cell development and that the CTR1 phenotype is not
the result of abnormal signalling in some other signalling
cascade which also includes CTRL
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Dolan—Pattern in the Root Epidermis
Since the synthesis of ACC is considered to be the rate
limiting step in ethylene biosynthesis the growth of roots in
the presence of ACC mimics treatment with ethylene (Yang
and Hoffman, 1984; Guzman and Ecker, 1990). Roots
grown in the presence of ACC developed hair cells in
ectopic locations, over the periclinal cell walls of cortical
cells (Fig. 2C) (Tanimoto, Roberts and Dolan, 1995). If
ethylene were a positive regulator of root hair cell development then it might be expected that the inhibition of
ethylene biosynthesis by AVG, and its perception of Ag+
would result in the development of fewer root hair cells (Fig.
2D). Both treatments result in the development of fewer
root hair cells in a concentration dependent fashion
(Tanimoto et al., 1995).
Recessive mutations in the ROOT HAIR DEVELOPMENTS (RHD6) gene decrease the number of root hair
cells that develop (Masucci and Schiefelbein, 1994). This
phenotype closely resembles the morphology of roots treated
with AVG and can be partially rescued by ACC. It remains
to be seen if the RHD6 gene is involved at the level of
ethylene biosynthesis or perception. Nevertheless it clearly
plays an important role in the development of hair cells.
These results are consistent with ethylene being a positive
regulator of root hair development. An important feature of
these results is that upon external application of ethylene
any cell in the epidermis can develop as a root hair cell. This
suggests that during normal development certain cells in the
epidermis are exposed to the inductive ethylene signal while
others are not. Those cells that are exposed to ethylene
develop as hair cells and those that are not develop as nonhair cells. The non-hair cell state might then be considered
the default pathway. Since those cells that respond to
ethylene and consequently form root hairs lie over the cleft
between two underlying cortical cells it is tempting to think
that the differential exposure to the positive inductive signal
results purely from the position of these cells (due to the
cellular geometry) relative to a signal originating from
within the root.
Reciprocal regulation of hair development in roots and
shoots
A number of genes involved in the development of hair
cells of the shoot—trichomes—have been identified by
mutation (Hiilskamp, Misera and Jiirgens, 1994). Two
positive regulators of trichome development, GLABRA1
(GL1) and GLABRA2 (GL2) have been cloned (Oppenheimer et al., 1991; Rerie, Feldman and Marks, 1994). They
encode transcriptional regulators of the myb and homoedomain families, respectively. TRANSPARENT
TESTA
GLABRA (TTG) is a further positive regulator of trichome
development, that as yet remains uncharacterized at the
molecular level (Koornneef, 1981). Since the role of these
genes in the development of hairs in the shoot epidermis has
been well characterized it was an obvious place to start
looking for potential regulators of hair development in the
root. Recessive alleles at the GL2 and TTG loci produce
root hair cells in ectopic locations (Dolan, unpubl. res.;
Galway et al., 1994). In addition, the cellular organization
of ttg root tip is abnormal, resembling roots in which the
quiescent centre is absent (Galway et al., 1994; Dolan
unpubl. res.). Nevertheless ttg plants go on to form roots
with normal cellular architecture. It is not clear if the
abnormal cellular organization is causally related to the
ectopic root hair phenotype or whether it is simply an
unrelated pleiotropic effect since ttg is known to have a
number of such effects in other parts of the plant (ttg plants
lack trichomes, anthocyanin and seed mucilage) (Koornneef,
1981).
Constitutive expression of the maize R-Lc gene using the
Cauliflower mosaic virus 35S promoter in Arabidopsis has
been shown to complement the ttg defect in trichome
development (Lloyd, Walbot and Davies, 1992). 35S-R-Lc
expressing plants form many more trichomes than wild-type
and in locations that are usually devoid of trichomes. This
suggests that this gene acts at or after ttg in the
developmental pathway leading to the development of
trichomes. As might be expected, constitutive expression of
the 35S-R-Lc gene in roots results in the development of
fewer root hair cells (Galway et al., 1994). Roots of ttg
plants, expressing 35S-R-Lc are hairless again indicating
that the R-Lc effect occurs at or later than ttg in the
developmental pathway (Galway et al., 1994).
A M O D E L FOR E P I D E R M A L P A T T E R N I N G
IN THE ARABIDOPSIS
ROOT
The mechanism of cell patterning in the root epidermis
involves ethylene, its biosynthetic genes and genes involved
in ethylene signal transduction. In addition, there are
negative regulatory genes of hair cell development that are
also involved in the development of shoot trichomes. Many
genes remain to be identified since mutant screens are still
far from saturated. The arrangement of these genes in a
meaningful pathway requires their epistatic interactions to
be determined. Unfortunately the results of these studies are
not yet available. In the absence of such data we must piece
together the available information as best we can to provide
an explanation for the development of pattern in Arabidopsis
root epidermis.
All cells in the epidermis of Ctrl roots lack or have reduced
levels of CTR1 activity. Since cells in any location in the
epidermis of such roots develop as hair cells it suggests that
CTR1 is inactive in root hair cells and active in the non-hair
cells during wild-type development. The formation of hairs
in the epidermal cells overlying the cleft between underlying
cortical cells suggests that CTR1 is inactivated in cells in this
location. Genetic analysis of the ethylene signal transduction
cascade indicates that ethylene signalling involves the ETR1
mediated inactivation of negative regulator CTR1 (Bleecker
et al., 1988; Chang et al., 1993; Chang and Meyerowitz,
1995). Since we predict that CTR1 is active in cells over
cortical periclinal walls it suggests that these cells are not
exposed to inactivating effects of ethylene during wild type
development. Cells in the cleft between underlying anticlinal
cortical cell walls on the other hand appear to be exposed to
ethylene which thereby inactivates CTR1 resulting in the
production of a root hair cell during normal development.
Consistent with this interpretation is the observation that
cells that normally fail to make hairs do so upon exposure
Dolan—Pattern in the Root Epidermis
ACC/Ethylene
FIG. 3. Model of epidermal differentiation in Arabidopsis. Differential
stimulation of epidermal cells by ethylene as a result of differential
sensitivity or differential exposure result in the inactivation of CTR1 in
the cell lying in the cleft, resulting in the development of a hair cell in
this position. GL2 and TTG are not included in this figure since their site
of action is unknown.
to ethylene. In addition, blocking either the synthesis or
perception of ethylene with either AVG or silver inhibits the
development of hair cells in any location.
The pattern of hairs in the Arabidopsis root epidermis
may be in part explained by differential exposure of
epidermal cells to ethylene (Fig. 3). This differential exposure
may be a consequence of the cellular architecture of the root
since cells lying over the space between underlying cell files
are exposed to the signal. Analysing the pattern of expression
of ethylene biosynthetic genes will be instructive in this
respect. It also remains to be seen what the putative
diffusible signal is. Is the signal ACC or ethylene? Our
model predicts that whichever it is, it may move through the
intercellular space between underlying cortical cells. ACC
has been shown to move over large distances in the apoplast
and ACC oxidase activity has been localized to the
intercellular space (Bradford and Yang, 1980; Latche et al,
1992). The synthesis of ACC in the procambium, in response
to an auxin flux signal for example, and its subsequent
radial diffusion through the intercellular space would result
in the exposure of epidermal cells lying over the cleft to
relatively high ACC levels which may then be converted by
ACC oxidase to ethylene which may act locally.
While a genetic and physiological role of ethylene suggests
that potentially mobile signals, such as ACC or ethylene,
may be involved in regulating pattern in the root epidermis,
the analysis of ttg and gl2 mutations suggests that these
genes regulate such signalling events, act downstream of
such signalling events or are involved in parallel. For
example if they act upstream, they may regulate the pattern
of ethylene biosynthesis in the root or the sensitivity of
different epidermal cells to ethylene. If they act downstream,
they may be transcriptional regulators that are inactivated
or transcriptionally repressed by ethylene in developing hair
cells. They may also act in parallel, with both signalling
pathways playing independent roles in the establishment of
pattern. Since GL2, a positive regulator of trichome
development, is highly expressed in trichomes and is a
negative regulator of root hair development we predict that
it and perhaps TTG are expressed in the non-hair files.
Ongoing studies will provide an insight as to how these
genes interact with ethylene.
Surgical experiments in which the developing epidermis
551
of Sinapis alba (Brassicaceae) was removed from underlying
cells resulted in the development of extranumerary hair cells
on the epidermis (Bunning, 1951; Barlow, 1984). These
observations suggest that during normal development, hair
cells are isolated from surrounding cells and thereby fail to
receive the signal that induces the development of non-hair
cells. Bunning (1951) concluded that the hair cell fate is the
default state. An alternative explanation might be that more
cells are exposed to the positive regulator of hair differentiation in surgically removed epidermis and that the nonhair cell fate is the default state. Such a model would be in
agreement with our model. In addition it is possible that the
production of ethylene in response to injury might be
expected to induce the development of ectopic root hair
cells.
Ethylene is a positive regulator of hair development in
many species
Our genetic and physiological studies clearly implicate
ethylene as playing a central role in the development of
pattern in the root epidermis of Arabidopsis. Since
Arabidopsis exhibits Type 3 hairs so characteristic of the
Brassicaceae it seems likely that it plays a positive regulatory
role in root epidermal development of other members of this
family. It is important to determine if the same signals are
involved in the establishment of epidermal pattern in species
that exhibit different modes of epidermal development.
Cormack (1937) identified ethylene as a potent inducer of
root hair cell development of a Elodea canadensis (Type 2).
In addition we have shown that blocking the ethylene
synthesis or perception inhibits the development of hairs in
the barley (Hordeum vulgare) (Type 2) (A. Barrett and
L. Dolan, unpubl. res.). Ethylene has been shown to be a
possible positive regulator of root hair cell development in
a number of dicotyledonous species exhibiting Type 1
development (Abeles, 1973). It remains to be seen if ethylene
is a positive regulator of root hair cell development among
members of the Lycopsida (clubmosses), Sphenopsida
(horsetails) and the Filopsida (ferns). Insight into the role of
ethylene in the development of root hair cells in these
systems will provide important insights into evolution of the
role of ethylene in epidermal patterning in plants.
If ethylene is a positive regulator of root hair cell
development in a wide range of species, how then can we
account for the differences in epidermal pattern observed in
these diverse groups of plants? Our model suggests that the
Arabidopsis pattern may emerge from restricted exposure of
epidermal cells to endogenously produced ethylene or by
the exposure of cells with different sensitivity to the
ethylene/ACC signal. Hair cells in the tomato root epidermis
undergo Type 1 development, i.e. any cell can form a root
hair. Root epidermal pattern might be explained in tomato
if the pattern of ethylene biosynthesis is less restricted in this
species than that proposed above for Arabidopsis. Consequently cells, irrespective of their position relative to
underlying cells, receive the inductive signal. It may be that
ethylene is only part of the story, as indeed it may be in
Arabidopsis, since it is possible that ethylene and TTG/GL2
interact to specify epidermal pattern. Cellular geometry
552
Dolan—Pattern in the Root Epidermis
may also be involved since the arrangement of cortical/
endodermal cells is irregular in tomato, unlike Arabidopsis,
where anticlinal cell walls in the cortex and endodermis are
arranged opposite each other and therefore form a direct
conduit between the stele and the epidermis (Cormack,
1947).
CONCLUSIONS
Leavitt (1904) described the differences in the patterns of
cell differentiation in the root epidermis of vascular plants.
Recently we have made steps towards a mechanistic
understanding of how patterning is established in
Arabidopsis. Genes encoding transcription factors and
elements of the ethylene signal transduction cascade have
indicated that ethylene or its precursor may be a diffusible
signal involved in the generation of the spatial pattern. The
examination of the role played by homologous genes from
other species with different patterns of epidermal cells will
elucidate the mechanism underpinning these other patterns
and how the mechanism has been modified during evolution.
ACKNOWLEDGEMENTS
I would like to thank my co-workers in the Root
Development Group for their invaluable help. In addition I
would like to thank Joe Ecker, Joe Kieber, Keith Roberts
and John Schiefelbein for invaluable discussions. I am also
most grateful for the critical comments of two anonymous
referees.
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